One Carbon Metabolism in SAR11 Pelagic Marine Bacteria
Publication Date
August 23, 2011
Journal
PLOS ONE
Authors
Jing Sun, Laura Steindler, J. Cameron Thrash, Kimberly H. Halsey, et al
Volume
6
Issue
8
Pages
e23973
DOI
https://dx.plos.org/10.1371/journal.pone.0023973
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0023973
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21886845
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3160333
Europe PMC
http://europepmc.org/abstract/MED/21886845
Web of Science
000294253500041
Scopus
80051997986
Mendeley
http://www.mendeley.com/research/one-carbon-metabolism-sar11-pelagic-marine-bacteria-2
Events
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Mendeley | Further Information

{"title"=>"One carbon metabolism in SAR11 pelagic marine bacteria", "type"=>"journal", "authors"=>[{"first_name"=>"Jing", "last_name"=>"Sun", "scopus_author_id"=>"55716210700"}, {"first_name"=>"Laura", "last_name"=>"Steindler", "scopus_author_id"=>"15521155600"}, {"first_name"=>"J. Cameron", "last_name"=>"Thrash", "scopus_author_id"=>"12797736000"}, {"first_name"=>"Kimberly H.", "last_name"=>"Halsey", "scopus_author_id"=>"8884524100"}, {"first_name"=>"Daniel P.", "last_name"=>"Smith", "scopus_author_id"=>"55139227900"}, {"first_name"=>"Amy E.", "last_name"=>"Carter", "scopus_author_id"=>"50261165600"}, {"first_name"=>"Zachary C.", "last_name"=>"Landry", "scopus_author_id"=>"36098067800"}, {"first_name"=>"Stephen J.", "last_name"=>"Giovannoni", "scopus_author_id"=>"7007043918"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-80051997986", "pui"=>"362405326", "doi"=>"10.1371/journal.pone.0023973", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"80051997986", "pmid"=>"21886845"}, "id"=>"a0faf25a-04e9-391f-a464-e9527b3102e9", "abstract"=>"The SAR11 Alphaproteobacteria are the most abundant heterotrophs in the oceans and are believed to play a major role in mineralizing marine dissolved organic carbon. Their genomes are among the smallest known for free-living heterotrophic cells, raising questions about how they successfully utilize complex organic matter with a limited metabolic repertoire. Here we show that conserved genes in SAR11 subgroup Ia (Candidatus Pelagibacter ubique) genomes encode pathways for the oxidation of a variety of one-carbon compounds and methyl functional groups from methylated compounds. These pathways were predicted to produce energy by tetrahydrofolate (THF)-mediated oxidation, but not to support the net assimilation of biomass from C1 compounds. Measurements of cellular ATP content and the oxidation of (14)C-labeled compounds to (14)CO(2) indicated that methanol, formaldehyde, methylamine, and methyl groups from glycine betaine (GBT), trimethylamine (TMA), trimethylamine N-oxide (TMAO), and dimethylsulfoniopropionate (DMSP) were oxidized by axenic cultures of the SAR11 strain Ca. P. ubique HTCC1062. Analyses of metagenomic data showed that genes for C1 metabolism occur at a high frequency in natural SAR11 populations. In short term incubations, natural communities of Sargasso Sea microbial plankton expressed a potential for the oxidation of (14)C-labeled formate, formaldehyde, methanol and TMAO that was similar to cultured SAR11 cells and, like cultured SAR11 cells, incorporated a much larger percentage of pyruvate and glucose (27-35%) than of C1 compounds (2-6%) into biomass. Collectively, these genomic, cellular and environmental data show a surprising capacity for demethylation and C1 oxidation in SAR11 cultures and in natural microbial communities dominated by SAR11, and support the conclusion that C1 oxidation might be a significant conduit by which dissolved organic carbon is recycled to CO(2) in the upper ocean.", "link"=>"http://www.mendeley.com/research/one-carbon-metabolism-sar11-pelagic-marine-bacteria-2", "reader_count"=>140, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>32, "Student > Doctoral Student"=>11, "Student > Ph. D. Student"=>42, "Student > Postgraduate"=>7, "Student > Master"=>19, "Other"=>6, "Student > Bachelor"=>15, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>32, "Student > Doctoral Student"=>11, "Student > Ph. D. Student"=>42, "Student > Postgraduate"=>7, "Student > Master"=>19, "Other"=>6, "Student > Bachelor"=>15, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Engineering"=>2, "Environmental Science"=>24, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>86, "Medicine and Dentistry"=>3, "Physics and Astronomy"=>1, "Chemistry"=>6, "Computer Science"=>3, "Immunology and Microbiology"=>2, "Earth and Planetary Sciences"=>5}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Chemistry"=>{"Chemistry"=>6}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>86}, "Computer Science"=>{"Computer Science"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>24}}, "reader_count_by_country"=>{"Sweden"=>2, "Hong Kong"=>1, "Belgium"=>1, "United States"=>4, "Finland"=>1, "Brazil"=>2, "Malaysia"=>1, "Chile"=>3, "Australia"=>1, "Nepal"=>1}, "group_count"=>5}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/744112"], "description"=>"<p>a. For each assay, cells were grown in media containing the test compound, then washed and starved for 20 hrs. Cellular ATP content was measured after cells were exposed for 2 hrs to the test compound (T), to no compound added (N), and to pyruvate (P; positive control to confirm metabolic activity of cells).</p><p>b. Asterisk indicates statistical significance (p-value <0.01) between “no compound added” and “test compound” treatments.</p>", "links"=>[], "tags"=>["starved", "cells", "c1", "methylated"], "article_id"=>414474, "categories"=>["Biochemistry", "Inorganic Chemistry", "Genetics", "Ecology", "Microbiology"], "users"=>["Jing Sun", "Laura Steindler", "J. Cameron Thrash", "Kimberly H. Halsey", "Daniel P. Smith", "Amy E. Carter", "Zachary C. Landry", "Stephen J. Giovannoni"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023973.t003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ATP_response_of_starved_cells_to_addition_of_C1_and_methylated_compounds_a_/414474", "title"=>"ATP response of starved cells to addition of C1 and methylated compounds<sup>a</sup>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-08-23 01:14:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/743775"], "description"=>"<p>Four paralogous AMTs in HTCC1062 were placed into three functional subgroups: DmdA-like, GcvT, and an AMT of unknown function. All four AMTs were also identified in HTCC1002 and HTCC7211 genomes. This phylogenetic tree was generated using the neighbor-joining method. Bootstrap values are based on 100 iterations.</p>", "links"=>[], "tags"=>["sar11", "amt"], "article_id"=>414142, "categories"=>["Biochemistry", "Inorganic Chemistry", "Genetics", "Ecology", "Microbiology"], "users"=>["Jing Sun", "Laura Steindler", "J. Cameron Thrash", "Kimberly H. Halsey", "Daniel P. Smith", "Amy E. Carter", "Zachary C. Landry", "Stephen J. Giovannoni"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023973.g004", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogeny_of_SAR11_AMT_proteins_/414142", "title"=>"Phylogeny of SAR11 AMT proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-23 01:09:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/743852"], "description"=>"<p>HTCC1062 Cells from log phase were collected and resuspended in artificial seawater media (ASW). Radioisotope assays were conducted at room temperature (22°C) in ASW amended with (A) 1 µM <sup>14</sup>C-[methyl]-GBT; (B) 5 µM <sup>14</sup>C-TMA; (C) 20 µM <sup>14</sup>C-methanol; or (D) 100 nM <sup>14</sup>C-formaldehyde. Where not visible, error bars are smaller than the size of the symbols.</p>", "links"=>[], "tags"=>["utilization", "htcc1062"], "article_id"=>414220, "categories"=>["Biochemistry", "Inorganic Chemistry", "Genetics", "Ecology", "Microbiology"], "users"=>["Jing Sun", "Laura Steindler", "J. Cameron Thrash", "Kimberly H. Halsey", "Daniel P. Smith", "Amy E. Carter", "Zachary C. Landry", "Stephen J. Giovannoni"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023973.g005", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_14_C_labeled_compound_utilization_by_HTCC1062_in_culture_/414220", "title"=>"<sup>14</sup>C-labeled compound utilization by HTCC1062 in culture.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-23 01:10:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/743594"], "description"=>"<p>(A) THF-linked oxidation pathway; (B) methanol oxidation pathway; (C) glycine betaine demethylation and oxidation; (D) methylamine oxidation pathways; (E) TMAO degradation pathway; (F) glycine cleavage pathway; (G) DMSP demethylation. Note: <b>?</b> - unidentified metabolic processes/enzymes; <b>*</b> - spontaneous reaction; <b>†</b> - two paralogous operons.</p>", "links"=>[], "tags"=>["c1", "methylated", "oxidation", "pathways", "sar11"], "article_id"=>413961, "categories"=>["Biochemistry", "Inorganic Chemistry", "Genetics", "Ecology", "Microbiology"], "users"=>["Jing Sun", "Laura Steindler", "J. Cameron Thrash", "Kimberly H. Halsey", "Daniel P. Smith", "Amy E. Carter", "Zachary C. Landry", "Stephen J. Giovannoni"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023973.g002", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proposed_C1_and_methylated_compound_oxidation_pathways_in_SAR11_Group_Ia_/413961", "title"=>"Proposed C1 and methylated compound oxidation pathways in SAR11 Group Ia.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-23 01:06:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/743444"], "description"=>"<p>(A) formate dehydrogenase; (B) methanol metabolism; (C) methylamine oxidation; (D) glycine betaine oxidation; (E) aminomethyltransferases (Asterisk). <b><i>fdhF</i></b>, formate dehydrogenase, alpha subunit; <b><i>fdsB</i></b>, NAD-dependent formate dehydrogenase, beta subunit; <b><i>fdhD</i></b><i>,</i> formate dehydrogenase, chain D; <b><i>mobA</i></b><i>,</i> molybdopterin-guanine dinucleotide biosynthesis protein A; <b><i>moeA</i></b>, molybdopterin biosynthesis protein; <b><i>fhs</i></b><i>,</i> formate-THF ligase; SAR11_1286, putative glutamine amidotransferase; <b>Fe-ADH,</b> iron-containing alcohol dehydrogenase; <b><i>ssdH,</i></b> aldehyde dehydrogenase family; SAR11_1289, short chain dehydrogenase; <b><i>soxB</i></b>, sarcosine oxidase; <b><i>soxD</i></b> & <b><i>soxD<sub>2</sub></i></b>, sarcosine oxidase delta chain; <b><i>soxA</i></b> & <b><i>soxA<sub>2</sub></i></b>, sarcosine oxidase alpha chain; <b><i>soxG</i></b> & <b><i>soxG<sub>2</sub></i></b>, sarcosine oxidase gamma subunit; <b><i>soxB</i></b><sub>2</sub>, sarcosine oxidase beta subunit; <b><i>glxBCD</i></b>, glutamate synthase; <b><i>glnT</i></b>, Glutamine synthetase III (putative gamma-glutamylmethylamide synthetase); <b><i>bhmT</i></b>, betaine-homocysteine methyltransferase; <b><i>sardh</i></b>, sarcosine dehydrogenase; <b><i>dmgdh</i></b>, dimethylglycine dehydrogenase; <b><i>gcvT</i></b><i>,</i> glycine system cleavage T-protein; <b><i>gcvH</i></b><i>,</i> glycine cleavage H-protein; <b><i>gcvP</i></b><i>,</i> glycine cleavage P-protein; <b><i>dmdA</i></b><i>,</i> dimethylsulfoniopropionate-dependent demethylase; <b><i>mhpC</i></b>, hydrolase, alpha/beta hydrolase fold family; <b><i>fadD</i></b>, CoA activator for DMSP beta oxidation; <b><i>mmgC</i></b><i>,</i> acyl-CoA dehydrogenase for DMSP beta oxidation; <b><i>metF,</i></b> methylene-THF reductase; <b><i>opuAB</i></b><i>,</i> glycine betaine transport system permease protein; <b><i>opuAA</i></b><i>,</i> glycine betaine transport ATP-binding protein; <b><i>opuAC</i></b><i>,</i> substrate-binding region of ABC-type glycine betaine transport system; SAR11_1265 & SAR11_1303, gcvT-like aminomethyltransferase protein; SAR11_1304, monomeric sarcosine oxidase. Colors correspond to pathways in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0023973#pone-0023973-g002\" target=\"_blank\">Figure 2</a>.</p>", "links"=>[], "tags"=>["c1", "oxidation", "regions", "htcc1062"], "article_id"=>413813, "categories"=>["Biochemistry", "Inorganic Chemistry", "Genetics", "Ecology", "Microbiology"], "users"=>["Jing Sun", "Laura Steindler", "J. Cameron Thrash", "Kimberly H. Halsey", "Daniel P. Smith", "Amy E. Carter", "Zachary C. Landry", "Stephen J. Giovannoni"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023973.g001", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Demethylation_and_C1_oxidation_regions_of_the_strain_HTCC1062_genome_/413813", "title"=>"Demethylation and C1 oxidation regions of the strain HTCC1062 genome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-23 01:03:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/743971"], "description"=>"<p>The oxidation and incorporation rates were calculated from the initial linear part of each curve. Rate of <sup>14</sup>C-compound oxidation to <sup>14</sup>CO<sub>2</sub> (▪); rate of <sup>14</sup>C-compounds incorporation into biomass (□).</p>", "links"=>[], "tags"=>["c1", "methylated", "compounds", "bacterioplankton", "sargasso"], "article_id"=>414339, "categories"=>["Biochemistry", "Inorganic Chemistry", "Genetics", "Ecology", "Microbiology"], "users"=>["Jing Sun", "Laura Steindler", "J. Cameron Thrash", "Kimberly H. Halsey", "Daniel P. Smith", "Amy E. Carter", "Zachary C. Landry", "Stephen J. Giovannoni"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023973.g006", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Utilization_of_14_C_labeled_C1_and_methylated_compounds_by_bacterioplankton_in_the_western_Sargasso_Sea_/414339", "title"=>"Utilization of <sup>14</sup>C-labeled C1 and methylated compounds by bacterioplankton in the western Sargasso Sea.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-23 01:12:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/374839", "https://ndownloader.figshare.com/files/374849", "https://ndownloader.figshare.com/files/374861", "https://ndownloader.figshare.com/files/374872", "https://ndownloader.figshare.com/files/374883", "https://ndownloader.figshare.com/files/374896"], "description"=>"<div><p>The SAR11 <em>Alphaproteobacteria</em> are the most abundant heterotrophs in the oceans and are believed to play a major role in mineralizing marine dissolved organic carbon. Their genomes are among the smallest known for free-living heterotrophic cells, raising questions about how they successfully utilize complex organic matter with a limited metabolic repertoire. Here we show that conserved genes in SAR11 subgroup Ia (<em>Candidatus</em> Pelagibacter ubique) genomes encode pathways for the oxidation of a variety of one-carbon compounds and methyl functional groups from methylated compounds. These pathways were predicted to produce energy by tetrahydrofolate (THF)-mediated oxidation, but not to support the net assimilation of biomass from C1 compounds. Measurements of cellular ATP content and the oxidation of <sup>14</sup>C-labeled compounds to <sup>14</sup>CO<sub>2</sub> indicated that methanol, formaldehyde, methylamine, and methyl groups from glycine betaine (GBT), trimethylamine (TMA), trimethylamine N-oxide (TMAO), and dimethylsulfoniopropionate (DMSP) were oxidized by axenic cultures of the SAR11 strain <em>Ca.</em> P. ubique HTCC1062. Analyses of metagenomic data showed that genes for C1 metabolism occur at a high frequency in natural SAR11 populations. In short term incubations, natural communities of Sargasso Sea microbial plankton expressed a potential for the oxidation of <sup>14</sup>C-labeled formate, formaldehyde, methanol and TMAO that was similar to cultured SAR11 cells and, like cultured SAR11 cells, incorporated a much larger percentage of pyruvate and glucose (27–35%) than of C1 compounds (2–6%) into biomass. Collectively, these genomic, cellular and environmental data show a surprising capacity for demethylation and C1 oxidation in SAR11 cultures and in natural microbial communities dominated by SAR11, and support the conclusion that C1 oxidation might be a significant conduit by which dissolved organic carbon is recycled to CO<sub>2</sub> in the upper ocean.</p> </div>", "links"=>[], "tags"=>["carbon", "metabolism", "sar11", "pelagic"], "article_id"=>134018, "categories"=>["Biochemistry", "Inorganic Chemistry", "Genetics", "Ecology", "Microbiology"], "users"=>["Jing Sun", "Laura Steindler", "J. Cameron Thrash", "Kimberly H. Halsey", "Daniel P. Smith", "Amy E. Carter", "Zachary C. Landry", "Stephen J. Giovannoni"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0023973.s001", "https://dx.doi.org/10.1371/journal.pone.0023973.s002", "https://dx.doi.org/10.1371/journal.pone.0023973.s003", "https://dx.doi.org/10.1371/journal.pone.0023973.s004", "https://dx.doi.org/10.1371/journal.pone.0023973.s005", "https://dx.doi.org/10.1371/journal.pone.0023973.s006"], "stats"=>{"downloads"=>19, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/One_Carbon_Metabolism_in_SAR11_Pelagic_Marine_Bacteria/134018", "title"=>"One Carbon Metabolism in SAR11 Pelagic Marine Bacteria", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-08-23 01:06:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/743696"], "description"=>"<p>Coloration is according to 16S rRNA gene phylogeny, as shown in the boxed legend. Bootstrap values were omitted for clarity; nodes with less than 60% support were collapsed. Arrows indicate Fe-ADH proteins for which methanol dehydrogenase activity has been demonstrated experimentally. Scale bar  = 0.4 changes per position.</p>", "links"=>[], "tags"=>["fe-adh"], "article_id"=>414064, "categories"=>["Biochemistry", "Inorganic Chemistry", "Genetics", "Ecology", "Microbiology"], "users"=>["Jing Sun", "Laura Steindler", "J. Cameron Thrash", "Kimberly H. Halsey", "Daniel P. Smith", "Amy E. Carter", "Zachary C. Landry", "Stephen J. Giovannoni"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023973.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_tree_of_Fe_ADH_proteins_/414064", "title"=>"Phylogenetic tree of Fe-ADH proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-23 01:07:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/744071"], "description"=>"<p>a. For each assay, cells were grown in media containing the test compound, then washed and starved for 20 hrs. Cellular ATP content was measured after cells were exposed for 2 hrs to the test compound (T), to no compound added (N), and to pyruvate (P; positive control to confirm metabolic activity of cells).</p><p>b. Asterisk indicates statistical significance (p-value <0.01) between “no compound added” and “test compound” treatments.</p>", "links"=>[], "tags"=>["starved", "cells"], "article_id"=>414442, "categories"=>["Biochemistry", "Inorganic Chemistry", "Genetics", "Ecology", "Microbiology"], "users"=>["Jing Sun", "Laura Steindler", "J. Cameron Thrash", "Kimberly H. Halsey", "Daniel P. Smith", "Amy E. Carter", "Zachary C. Landry", "Stephen J. Giovannoni"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023973.t002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ATP_response_of_starved_cells_to_addition_of_various_alcohols_a_/414442", "title"=>"ATP response of starved cells to addition of various alcohols<sup>a</sup>.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-08-23 01:14:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/744037"], "description"=>"<p>The phylogenomics pipeline HAL and manual searches were used to detect orthologs among the genomes. Genes for C1 oxidation were present in all three genomes. HTCC7211 possesses three genes for the glutathione (GSH) dependent C1 oxidation pathway that are not present in the other two SAR11 Ia genomes.</p>", "links"=>[], "tags"=>["genes", "c1", "metabolism", "sar11", "ia"], "article_id"=>414405, "categories"=>["Biochemistry", "Inorganic Chemistry", "Genetics", "Ecology", "Microbiology"], "users"=>["Jing Sun", "Laura Steindler", "J. Cameron Thrash", "Kimberly H. Halsey", "Daniel P. Smith", "Amy E. Carter", "Zachary C. Landry", "Stephen J. Giovannoni"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023973.t001", "stats"=>{"downloads"=>3, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_genes_involved_in_C1_metabolism_among_three_SAR11_Ia_genomes_/414405", "title"=>"Distribution of genes involved in C1 metabolism among three SAR11 Ia genomes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-08-23 01:13:25"}

PMC Usage Stats | Further Information

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Relative Metric

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